Michael P. Lesser

Sponges are important ecological and functional components of coral reefs. Recently, a new hypothesis about the functional ecology of sponges in organic matter recycling pathways, the sponge-loop hypothesis, in which dissolved and particulate organic matter is taken up by sponges and shunted to higher trophic levels as detritus, has been proposed and demonstrated for shallow (< 30 m) cryptic species. However, support for this hypothesis at mesophotic depths (∼ 30–150 m) is lacking. Here, we examined detritus production, a prerequisite of the sponge loop pathway, in a reciprocal transplant experiment, using Halisarca caerulea from water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples of H. caerulea. Additionally, detritus production rates in transplanted sponges moved in the direction of rates observed for resident conspecifics. The microbiome of these sponge populations was also significantly different between shallow and mesophotic depths, and the microbial communities of the transplanted sponges also shifted in the direction of their new depth in 10 d largely driven by changes in Oxyphotobacteria, Acidimicrobiia, Nitrososphaeria, Nitrospira, Deltaproteobacteria, and Dadabacteriia. This occurred in an environment where the availability of both dissolved and particulate trophic resources changed significantly across the shallow to mesophotic depth gradient where these sponge populations were found. These results suggest that changes in sponge detritus production are primarily driven by differential quality and quantity of trophic resources, as well as their utilization by the sponge host, and its microbiome, along the shallow to mesophotic depth gradient.

Abstract

Background: The importance of symbiosis has long been recognized on coral reefs, where the photosynthetic dinof lagellates of corals (Symbiodiniaceae) are the primary symbiont. Numerous studies have now shown that a diverse assemblage of prokaryotes also make-up part of the microbiome of corals. A subset of these prokaryotes is capable of f ixing nitrogen, known as diazotrophs, and is also present in the microbiome of scleractinian corals where they have been shown to supplement the holobiont nitrogen budget. Here, an analysis of the microbiomes of 16 coral species collected from Australia, Curaçao, and Hawai’i using three different marker genes (16S rRNA, nifH, and ITS2) is presented. These data were used to examine the effects of biogeography, coral traits, and ecological life history characteristics on the composition and diversity of the microbiome in corals and their diazotrophic communities.

Results: The prokaryotic microbiome community composition (i.e., beta diversity) based on the 16S rRNA gene varied between sites and ecological life history characteristics, but coral morphology was the most significant factor affecting the microbiome of the corals studied. For 15 of the corals studied, only two species Pocillopora acuta and Seriotopora hystrix, both brooders, showed a weak relationship between the 16S rRNA gene community structure and the diazotrophic members of the microbiome using the nifH marker gene, suggesting that many corals support a microbiome with diazotrophic capabilities. The order Rhizobiales, a taxon that contains primarily diazotrophs, are common members of the coral microbiome and were eight times greater in relative abundances in Hawai’i compared to corals from either Curacao or Australia. However, for the diazotrophic component of the coral microbiome, only host species significantly influenced the composition and diversity of the community.

Conclusions: The roles and interactions between members of the coral holobiont are still not well understood, especially critical functions provided by the coral microbiome (e.g., nitrogen fixation), and the variation of these functions across species. The findings presented here show the significant effect of morphology, a coral “super trait,” on the overall community structure of the microbiome in corals and that there is a strong association of the diazotrophic community within the microbiome of corals. However, the underlying coral traits linking the effects of host species on diazotrophic communities remain unknown.

Abstract

Sponges are a diverse phylum of sessile filter-feeding invertebrates that are abundant on Caribbean reefs and provide essential ecological services, including nutrient cycling, reef stabilization, habitat, and food for a variety of fishes and invertebrates. As prominent members of the benthic community, and thus potential food resources, factors determining the biochemical and energetic content of sponges will affect their trophic contributions to coral reef ecosystems. In order to evaluate the influence of geographic variation on biochemical composition and energetic content in the tissue of sponges, we collected several common and widespread species (Agelas conifera, Agelas tubulata, Amphimedon compressa, Aplysina cauliformis, Niphates amorpha, Niphates erecta, and Xestospongia muta) from multiple shallow reefs in four countries across the Caribbean Basin, including Belize, Curaçao, Grand Cayman, and St. Croix, U.S. Virgin Islands. In addition, we correlated inherent species-level traits, including the production of antipredator chemical defenses and the relative abundance of microbial symbionts, with biochemical and energetic content. We found that energetic content was higher in sponges with antipredator chemical defenses, and was significantly correlated with the concentration of chemical extracts from these sponges. We also noted that sponges with high microbial abundance contained significantly more soluble protein than sponges with low microbial abundance. Finally, both biochemical and energetic content varied significantly among sponges from different locations; sponges from Grand Cayman had the highest lipid and energetic content, whereas sponges from Belize had the highest carbohydrate content but lowest energetic content. Despite similar environmental conditions at these sites, our results demonstrate that biochemical and energetic content of sponges exhibits geographic variability, with potential implications for the trophic ecology of sponges throughout the Caribbean Basin.

https://doi.org/10.1111/ivb.12341